Schultheiß et al. BMC Evolutionary Biology 2014, 14:42 http://www.biomedcentral.com/1471-2148/14/42 RESEARCH ARTICLE Open Access Disjunct distributions of freshwater snails testify to a central role of the Congo system in shaping biogeographical patterns in Africa Roland Schultheiß1,2*, Bert Van Bocxlaer3,4, Frank Riedel5,6, Thomas von Rintelen7 and Christian Albrecht2 Abstract Background: The formation of the East African Rift System has decisively influenced the distribution and evolution of tropical Africa’s biota by altering climate conditions, by creating basins for large long-lived lakes, and by affecting the catchment and drainage directions of river systems. However, it remains unclear how rifting affected the biogeographical patterns of freshwater biota through time on a continental scale, which is further complicated by the scarcity of molecular data from the largest African river system, the Congo. Results: We study these biogeographical patterns using a fossil-calibrated multi-locus phylogeny of the gastropod family Viviparidae. This group allows reconstructing drainage patterns exceptionally well because it disperses very poorly in the absence of existing freshwater connections. Our phylogeny covers localities from major drainage basins of tropical Africa and reveals highly disjunct sister-group relationships between (a) the endemic viviparids of Lake Malawi and populations from the Middle Congo as well as between (b) the Victoria region and the Okavango/ Upper Zambezi area. Conclusions: The current study testifies to repeated disruptions of the distribution of the Viviparidae during the formation of the East African Rift System, and to a central role of the Congo River system for the distribution of the continent’s freshwater fauna during the late Cenozoic. By integrating our results with previous findings on palaeohydrographical connections, we provide a spatially and temporarily explicit model of historical freshwater biogeography in tropical Africa. Finally, we review similarities and differences in patterns of vertebrate and invertebrate dispersal. Amongst others we argue that the closest relatives of present day viviparids in Lake Malawi are living in the Middle Congo River, thus shedding new light on the origin of the endemic fauna of this rift lake. Keywords: Freshwater biogeography, East African Rift System, Congo, Lake Malawi, Lake Tanganyika, Zambezi Background The three largest drainage systems in present-day Cen- The formation of the East African Rift System (EARS) tral Africa are the Congo-, the Nile-, and the Zambezi played a decisive role in the evolution of Africa’s tropical system (Figure 1). The Congo River covers an area of ~3.7 fauna and flora. The climatic, geological, and hydrolo- million square kilometres and has a length of ~4100 ki- gical consequences of the rifting processes are critical to lometres [2]. It drains part of the EARS (including understand the emergence of the endemic species of the Lake Tanganyika) and borders to the Nile system in the savannahs and the Great Lakes as well as the origin of northeast. The Nile system receives water from Lake humankind. Rifting created, disrupted, redirected, and Albert and Lake Victoria and drains a region of ~3.2 connected major freshwater systems [1]. million square kilometres for almost 7000 kilometres northwards to the Mediterranean Sea. To the south, the * Correspondence: [email protected] Congo system borders to the Zambezi drainage system, 1Division of Genetics and Physiology, Department of Biology, University of which runs ~2600 kilometres, covers an area of 1.3 million Turku, Itäinen Pitkäkatu 4, 20014 Turku, Finland square kilometres [2,3], and includes the southernmost 2Department of Animal Ecology & Systematics, Justus Liebig University Giessen, Heinrich-Buff-Ring 26-32, Giessen 35392, Germany of the Great Lakes, Malawi. The central location of the Full list of author information is available at the end of the article EARS to these river systems bears witness to the rift’s © 2014 Schultheiß et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Schultheiß et al. BMC Evolutionary Biology 2014, 14:42 Page 2 of 12 http://www.biomedcentral.com/1471-2148/14/42 Nile Lake Albert drainage system ngo River im Co ruw i A Congo drainage system Lake Muhazi Lake Victoria Ka Lake Tanganyika sa i Lake Mweru N Okavango Lake Malawi drainage Lake Bangweulu system Zambezi drainage U system . Z mbezi O a Za k m a b v e a z n i sample locality g o lake river course Chobe drainage system border Lake 0 100 200 500 km Palaeo-Makgadikgadi Figure 1 Map of tropical Africa with major drainage systems. The map shows the major drainage systems, framed with bold grey lines, and the sampling points of the study. Lakes and rivers referred to in the text are labelled accordingly; the Upper Zambezi is abbreviated as ‘U. Zambezi’. The dashed outline indicates the maximum expansion of Lake Palaeo-Makgadikgadi, modified after Riedel et al. [4]. Locality details for each sampling point are given in Table 1. importance in shaping drainage pattern of tropical Africa, centre of the continent and palaeohydrological research but their history since the Mid-Miocene is only partly re- indicates that the river and its tributaries have a highly solved and arguably complex [2,3]. vicissitudinous drainage history. Temporal connections Most suggestions of palaeohydrological connections in existed to the present day Lake Victoria area [14,15], Lake tropical Africa are based on circumstantial evidence in Turkana [16,17], the Upper Zambezi area [18,19] and the combination with general models of rifting and uplifting Indian Ocean [19], although the latter connection is con- [2] rather than on geomorphological evidence like in other troversial [1]. Hence, the analysis of Congolese samples is parts of the continent where palaeochannels can be traced a prerequisite for our understanding of the evolution and over considerable areas and are reasonably well dated, e.g. distribution of the freshwater fauna of tropical Africa— [5-7]. The consequential lack of a coherent synthesis or including the origins of the endemic radiations in the rift- a model of hydrographical connections since the Mid- lakes Malawi and Tanganyika. Miocene severely hampers our understanding of historical Here we study the historical biogeography of the fresh- biogeography in tropical Africa. This is further compli- water gastropod family Viviparidae, a taxon widely dis- cated by a scarcity of samples from the Congo River sys- tributed in the lotic and lentic environments of tropical tem, e.g. [8-11], but see Goodier et al. [12] and Day et al. Africa [20]. This family is of particular interest to studies [13]. The Congo is the largest freshwater system in the of historical freshwater biogeography because its dispersal Schultheiß et al. BMC Evolutionary Biology 2014, 14:42 Page 3 of 12 http://www.biomedcentral.com/1471-2148/14/42 is mostly limited to habitats with existing freshwater con- nodes were collapsed into a polytomy in Figure 2. The nections [21], rendering it an ideal tracer of past and number of parsimony informative sites and effective sam- present hydrographic connections. The ovoviviparous and pling sizes are provided in Additional file 1 for each frag- dioecious reproduction mode of viviparids minimizes op- ment separately. portunities for successful vector-mediated migration and a The phylogenetic structure revealed by Figure 2 also subsequent establishment of a viable population [22,23]. indicates that morphological identifications and geneal- Accordingly, viviparid fossils are conspicuously absent ogy do not match each other perfectly. A main concern from African water bodies that were never hydrographic- is the systematic position of Bellamya capillata, which ally connected to a source, e.g. crater- and oasis lakes [21]. has been traditionally reported from many localities in We obtained samples from the major drainage systems Africa south of the equator [20]. The type locality for in the region, i.e. that of the Nile, the Okavango, the this taxon is Lake Malawi, and all other localities from Zambezi as well as the Upper and Middle Congo. Using which the species was identified, are in fact inhabited by Bayesian multi-locus phylogenetic analyses and a fossil- populations that are deeply divergent from B. capillata calibrated, relaxed molecular clock we studied the diver- in Lake Malawi. Similar issues exist for other Bellamya sification and distribution of viviparids in Africa. In light species (see Discussion). We thus tentatively name spec- of the impact of the evolution of the EARS on African imens with an ambiguous status in current systematics hydrographic systems and the dependence of our model using ‘confer’ (cf.) to emphasize that taxonomic revisions organism on these systems to disperse, we expect a deep are required. phylogenetic separation between viviparid species east and west of the western branch of the rift system. We Molecular clock estimates furthermore hypothesize this separation to temporarily We focus on estimates for the ages of the following coincide with the disruption of freshwater migration routes three nodes in Clade I (Figure 2): Split A—most recent across the evolving rift. common ancestor (mrca) of the entire clade: 10.47 mil- lion years (My) (95% confidence interval [CI]: 6.69-15.04 Results My); Split B—the split between the Victoria- and the Phylogenetic analyses Okavango group: 6.32 My (CI: 3.58-9.96 My); Split C— The Bayesian analyses of the African Viviparidae yiel- the split between the Congo- and the Malawi group: ded one well-supported Neothauma group from Lake 4.52 My (CI: 2.32-7.70 My).